Mosquito diapause

Annual Review of Entomology

Volumn 59, Issue , 2014, Pages 73-93

  Denlinger, David L ^a   Armbruster, Peter A ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

Aestivation; Disease transmission; Dormancy; Global warming; Insect seasonality; Population variation

Indexed keywords

INSECT HORMONE;

ANIMAL; DIAPAUSE; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; LARVA; MOSQUITO; OOCYTE; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; CULICIDAE; DIAPAUSE, INSECT; INSECT HORMONES; LARVA; OVUM; PUPA;

EID: 84891915952     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-011613-162023     Document Type: Article

References (121)

1. Anderson JF. 1968. Influence of photoperiod and temperature on the induction of diapause in Aedes atropalpus (Diptera, Culicidae). Entomol. Exp. Appl. 11:321-30
2. Andrewartha HG. 1952. Diapause in relation to the ecology of insects. Biol. Rev. 27:50-107
3. Baqar S, Hayes CG, Murphy JR, Watts DM. 1993. Vertical transmission of West Nile virus by Culex and Aedes species mosquitoes. Am. J. Trop. Med. Hyg. 48:757-62
4. Barnard DR, Mulla MS. 1978. The ecology of Culiseta inornata in the Colorado desert of California: Seasonal abundance, gonotrophic status, and oviparity of adult mosquitoes. Ann. Entomol. Soc. Am. 71:397-400
5. Beach RF. 1978. The required day number and timely induction of diapause in geographic strains of the mosquito, Aedes atropalpus. J. Insect Physiol. 24:449-55
6. Bean DW, Dalin P, Dudley TL. 2012. Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp). Evol. Appl. 5:511-23
7. Beckel WE. 1958. Investigations of permeability, diapause, and hatching in eggs of the mosquito Aedes hexodontus Dyar. Can. J. Zool. 36:541-55
8. Benoit JB. 2010. Water management by dormant insects: Comparisons between dehydration resistance during summer aestivation and winter diapause. In Aestivation: Molecular and Physiological Aspects, ed.CA Navas, JE Caralho, pp. 209-29. Berlin: Springer
9. Benoit JB, Denlinger DL. 2007. Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J. Exp. Biol. 210:217-26
10. Black WC, Moore CG. 2005. Population biology as a tool to study vector-borne disease. In Biology of Disease Vectors, ed. WC Marquardt, pp. 187-206. Burlington, MA: Elsevier Academic
11. Bowen MF. 1992. Patterns of sugar feeding in diapausing and nondiapausing Culex pipiens (Diptera: Culicidae) females. J. Med. Entomol. 29:843-49
12. Bowen MF, Davis EE, Haggart DA. 1988. A behavioral and sensory analysis of host-seeking behavior in the diapausing mosquito Culex pipiens (Diptera: Culicidae) females. J. Insect Physiol. 34:805-13
13. BradshawWE.1976. Geography of photoperiodic response in a diapausing mosquito. Nature 262:384-86
14. Bradshaw WE, Armbruster P, Holzapfel CM. 1998. Fitness consequences of hibernal diapause in the pitcher-plant mosquito, Wyeomyia smithii. Ecology 79:1458-62
15. Bradshaw WE, Emerson KJ, Catchen JM, CreskoWA, Holzapfel CM. 2012. Footprints in time: Comparative quantitative trait loci mapping of the pitcher-plant mosquito, Wyeomyia smithii. Proc. R. Soc. B 279:4551-58
16. Bradshaw WE, Haggerty BP, Holzapfel CM. 2005. Epistasis underlying a fitness trait within a natural population of the pitcher-plant mosquito, Wyeomyia smithii. Genetics 169:485-88
17. Bradshaw WE, Holzapfel CM. 1977. Interaction between photoperiod, temperature and chilling in dormant larvae of the tree-hole mosquito, Toxorhynchites rutilus Coq. Biol. Bull. 152:147-58
18. Bradshaw WE, Holzapfel CM. 1992. Resource limitation, habitat segregation, and species interactions of British tree-hole mosquitoes in nature. Oecologia 90:227-37
19. Bradshaw WE, Holzapfel CM. 2001. Genetic shift in photoperiodic response correlated with global warming. Proc. Natl. Acad. Sci. USA 98:14509-11
20. Bradshaw WE, Holzapfel CM. 2010. Light, time, and the physiology of biotic response to rapid climate change in animals. Annu. Rev. Physiol. 72:147-66
21. BradshawWE,Lounibos LP. 1972. Photoperiodic control of development in the pitcher-plantmosquito, Wyeomyia smithii. Can. J. Zool. 50:713-19
22. BradshawWE,Lounibos LP. 1977. Evolution of dormancy and its photoperiodic control in pitcher-plant mosquitoes. Evolution 31:546-67
23. Bradshaw WE, Zani PA, Holzapfel CM. 2004. Adaptation to temperate climates. Evolution 58:1748-62
24. Coluzzi M, Di Deco M, Gironi A. 1975. The influence of photoperiod on the selection of oviposition sites in Aedes mariae (Diptera: Culicidae). Parassitologia 17:121-30
25. Danks HV. 1987. Insect Dormancy: An Ecological Perspective. Ottawa: Biol. Surv. Can. (Terrestrial Arthropods
26. Das S, Dimopoulos G. 2008. Molecular analysis of photic inhibition of blood-feeding in Anopheles gambiae. BMC Physiol. 8:23
27. Denlinger DL. 1974. Diapause potential in tropical flesh flies. Nature 252:223-24
28. Denlinger DL. 1986. Dormancy in tropical insects. Annu. Rev. Entomol. 31:239-64
29. Denlinger DL. 2002. Regulation of diapause. Annu. Rev. Entomol. 47:93-122
30. Denlinger DL, Giebultowicz J, Adedokun T. 1988. Insect diapause: Dynamics of hormone sensitivity and vulnerability to environmental stress. In Endocrinological Frontiers in Physiological Insect Ecology, ed. F Sehnal, A Zabza, DL Denlinger, pp. 885-98. Wroclaw, Poland: Wroclaw Tech. Univ. Press
31. Denlinger DL, Lee RE. 2010. Low Temperature Biology of Insects. Cambridge, UK: Cambridge Univ. Press
32. Denlinger DL, Yocum GD, Rinehart JP. 2012. Hormonal control of diapause. In Insect Endocrinology, ed. LI Gilbert, pp. 430-63. San Diego, CA: Academic
33. Eldridge BF. 1968. The effect of temperature and photoperiod on blood-feeding and ovarian development in mosquitoes of the Culex pipiens complex. Am. J. Trop. Med. Hyg. 17:133-40
34. Eldridge BF, Johnson MD, Bailey CL. 1976. Comparative studies of two North American mosquito species, Culex restuans and Culex salinarius: Response to temperature and photoperiod in the laboratory. Mosq. News 36:506-13
35. EmersonKJ, Bradshaw WE,Holzapfel CM. 2010. Microarrays reveal early transcriptional events during the termination of larval diapause in natural populations of the mosquito, Wyeomyia smithii. PLoS One 5:e9574
36. Emerson KJ, Uyemura AM, McDaniel KL, Schmidt PS, BradshawWE, Holzapfel CM. 2009. Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster. J. Comp. Physiol. A 195:825-29
37. Evans KW, Brust RA. 1972. Induction and termination of diapause in W. smithii (Diptera: Culicidae), and larval survival studies at low and sub-zero temperatures. Can. Entomol. 104:1937-50
38. Focks DA, Linda SB, Craig GBJ, Hawley WA, PumpuniCB. 1994. Aedes albopictus (Diptera:Culicidae): A statistical model of the role of temperature, photoperiod, and geography in the induction of egg diapause. J. Med. Entomol. 31:278-86
39. Frohne WC. 1953. Natural history of Culiseta impatiens (Wlk), (Diptera, Culicidae) in Alaska. Trans. Am. Microsc. Sci. 72:103-18
40. Frohne WC. 1954. Biology of an Alaskan mosquito, Culiseta alaskaensis (Ludl). Ann. Entomol. Soc. Am. 47:9-24
41. Gentile C, Rivas GBS,Meireles ACA, Lima JBP, Peixoto AA. 2009. Circadian expression of clock genes in two mosquito disease vectors: Cry2 is different. J. Biol. Rhythms 24:444-51
42. Goto SG, Shiga S, Numata H. 2010. Photoperiodism in insects: Perception of light and the role of clock genes. In Photoperiodism: The Biological Calendar, ed. RJ Nelson, DL Denlinger, DE Somers, pp. 258-86. Oxford, UK: Oxford Univ. Press
43. Hahn DA, Denlinger DL. 2011. Energetics of insect diapause. Annu. Rev. Entomol. 56:103-21
44. Hanson SM, Craig GBJ. 1995. Aedes albopictus (Diptera: Culicidae) eggs: Field survivorship during northern Indiana winters. J. Med. Entomol. 32:599-604
45. Hard JJ, Bradshaw WE, Holzapfel CM. 1992. Epistasis and the genetic divergence of photoperiodism between populations of the pitcher-plant mosquito, Wyeomyia smithii. Genetics 131:389-96
46. Hawley WA, Reiter P,Copeland RS, PumpuniCB, Craig GB Jr. 1987. Aedes albopictus in North America: Probable introduction in used tires from northern Asia. Science 236:1114-16
47. Holzapfel CM, Bradshaw WE. 1981. Geography of larval dormancy in the tree-hole mosquito, Aedes triseriatus (Say). Can. J. Zool. 59:1014-21
48. Horsfall WR, Fowler HWJ. 1961. Eggs of floodwater mosquitoes. VIII. Effect of serial temperatures on conditioning of eggs of Aedes stimulans Walker (Diptera: Culicidae). Ann. Entomol. Soc. Am. 54:664-66
49. HorsfallWR,Trpis M. 1967. Eggs of floodwater mosquitoes.X.Conditioning and hatching of winterized eggs of Aedes sticticus (Diptera: Culicidae). Ann. Entomol. Soc. Am. 60:1021-25
50. Huestis DL, Yaro AS, Traore AI, Dieter KL, Nwagbara JI, et al. 2012. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J. Exp. Biol. 215:2013-21
51. Jordan RG. 1980. Embryonic diapause in three populations of the western tree hole mosquito, Aedes sierrensis. Ann. Entomol. Soc. Am. 73:357-59
52. Jordan RG, Bradshaw WE. 1978. Geographic variation in the photoperiodic response of the western tree-hole mosquito, Aedes sierrensis. Ann. Entomol. Soc. Am. 71:787-90
53. Joy JE, Sullivan SN. 2005. Occurrence of tire inhabiting mosquito larvae in different geographic regions of West Virginia. J. Am. Mosq. Control Assoc. 21:380-86
54. Juliano SA. 2009. Species interactions among larval mosquitoes: Context dependence across habitat gradients. Annu. Rev. Entomol. 54:37-56
55. Juliano SA, Lounibos LP. 2005. Ecology of invasive mosquitoes: Effects on resident species and human health. Ecol. Lett. 8:558-74
56. Juliano SA, O'Meara GF, Morrill JR, Cutwa MM. 2002. Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia 130:458-69
57. Kim M, Denlinger DL. 2009. Decrease in expression of the beta-Tubulin and microtubule abundance in flight muscles during diapause in adults of Culex pipiens. Insect Mol. Biol. 18:295-302
58. Kim M, Denlinger DL. 2010. A potential role for ribosomal protein S2 in the gene network regulating reproductive diapause in the mosquito Culex pipiens. J. Comp. Physiol. B 180:171-78
59. Kim M, Robich RM, Rinehart JP, Denlinger DL. 2006. Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J. Insect Physiol. 52:1226-33
60. Kim M, Sim C, Denlinger DL. 2010. RNA interference directed against ribosomal protein S3a suggests a link between this gene and arrested ovarian development during adult diapause in Culex pipiens. Insect Mol. Biol. 19:27-33
61. Kostal V. 2011. Insect photoperiodic calendar and circadian clock: Independence, cooperation, or unity? J. Insect Physiol. 57:538-56
62. Lair KP, Bradshaw WE, Holzapfel CM. 1997. Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 147:1873-83
63. Lee K-Y, Denlinger DL. 1997. A role for ecdysteroids in the induction and maintenance of the pharate first instar diapause of the gypsy moth, Lymantria dispar. J. Insect Physiol. 43:289-96
64. Lehmann T, Dao A, Yaro AS, Adamou A, Kassogue T, et al. 2010. Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Am. J. Trop. Med. Hyg. 83:601-6
65. Li AQ,DenlingerDL. 2009. Pupal cuticle protein is abundant during early adult diapause in themosquito Culex pipiens. J. Med. Entomol. 46:1382-86
66. Livdahl TP, WilleyMS. 1991. Prospects for an invasion: Competition between Aedes albopictus and native Aedes triseriatus. Science 253:189-91
67. Lounibos LP, Bradshaw WE. 1975. A second diapause in Wyeomyia smithii: Seasonal incidence and maintenance by photoperiod. Can. J. Zool. 53:215-21
68. Lounibos LP, Escher RL, Lourenco-De-Oliveira R. 2003. Asymmetric evolution of photoperiodic diapause in temperate and tropical invasive populations of Aedes albopictus (Diptera:Culicidae). Ann. Entomol. Soc. Am. 96:512-18
69. Lounibos LP, Escher RL, NishimuraN. 2011. Retention and adaptiveness of photoperiodic egg diapause in Florida populations of invasive Aedes albopictus. J. Am. Mosq. Control Assoc. 27:433-36
70. MacRae TH. 2010. Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 67:2405-24
71. Mathias D, Jacky L, Bradshaw WE, Holzapfel CM. 2005. Geographic and developmental variation in expression of the circadian rhythm gene, timeless, in the pitcher-plant mosquito, Wyeomyia smithii. J. Insect Physiol. 51:661-67
72. Mathias D, Jacky L, Bradshaw WE, Holzapfel CM. 2007. Quantitative trait loci associated with photoperiodic response and stage of diapause in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 176:391-402
73. MeutiME, DenlingerDL. 2013. Evolutionary links between circadian clocks and photoperiodic diapause in insects. Integr. Comp. Biol. 53:131-43
74. Mitchell CJ. 1988. Occurrence, biology and physiology of diapause in overwintering mosquitoes. In The Arboviruses: Epidemiology and Ecology, Vol. 1, ed. TP Monath, pp. 191-217. Boca Raton, FL: CRC Press
75. Mitchell CJ, Briegel H. 1989. Fate of the blood meal in force-fed, diapausing Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 26:332-41
76. Mitchell CJ, Briegel H. 1989. Inability of diapausing Culex pipiens (Diptera: Culicidae) to use blood for producing lipid reserves for overwinter survival. J. Med. Entomol. 26:318-26
77. Mori A, Romero-Severson J, Severson DW. 2007. Genetic basis for reproductive diapause is correlated with life history traits within the Culex pipiens complex. Insect Mol. Biol. 16:515-24
78. Nasci RS, Savage HM, White DJ, Miller JR, Cropp BC, et al. 2001. West Nile virus in overwintering Culex mosquitoes, New York City, 2000. Emerg. Infect. Dis. 7:742-44
79. Parker BM. 1985. Effects of photoperiod on the induction of embryonic diapause in Aedes taeniorhynchus (Diptera: Culicidae). J. Med. Entomol. 22:392-97
80. Parker BM. 1988. Photoperiod-induced diapause in a North Carolina strain of Aedes sollicitans: Photosensitivity of fully formed and developing embryos. J. Am. Mosq. Control Assoc. 4:57-63
81. Perez MH, Noriega FG. 2013. Aedes aegypti pharate 1st instar quiescence: A case for anticipatory reproductive plasticity. J. Insect Physiol. 59:318-24
82. Poelchau M, Reynolds J, Denlinger D, Elsik C, Armbruster P. 2011. A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation. BMC Genomics 12:619
83. Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA. 2013. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B 280:20130143
84. Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA. 2013. RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus. J. Exp. Biol. 216:4082-90
85. Ptitsyn AA, Reyes-Solis G, Saavedra-Rodriguez K, Betz J, Suchman EL, et al. 2011. Rhythms and synchronization patterns in gene expression in the Aedes aegypti mosquito. BMC Genomics 12:153
86. Pumpuni CB. 1989. Factors influencing photoperiodic control of egg diapause in Aedes albopictus (Skuse). PhD Thesis. Univ. Notre Dame, Notre Dame, Indiana. 148 pp.
87. Pumpuni CB, Knepler J, Craig GB. 1992. Influence of temperature and larval nutrition on the diapause inducing photoperiod of Aedes albopictus. J. Am. Mosq. Control Assoc. 14:223-27
88. Ragland GJ, Denlinger DL, Hahn DA. 2010. Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc. Natl. Acad. Sci. USA 17:14909-14
89. Ragland GJ, Egan SP, Feder JL, Berlocher SH, Hahn DA. 2011. Developmental trajectories of gene expression reveal candidates for diapause termination: A key life-history transition in the apple maggot fly Rhagoletis pomonella. J. Exp. Biol. 214:3948-59
90. Readio J, Chen MH, Meola R. 1999. Juvenile hormone biosynthesis in diapausing and nondiapausing Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 36:355-60
91. Reidenbach KR, Cook S, Bertone MA, Harbach RE,Wiegmann BM, Besansky NJ. 2009. Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evol. Biol. 9:298
92. Reynolds JA, Poelchau MF, Rahman Z, Armbruster PA, Denlinger DL. 2012. Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. J. Insect Physiol. 58:966-73
93. Rinehart JP, Li A, Yocum GD, Robich RM,Hayward SAL, Denlinger DL. 2007. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc. Natl. Acad. Sci. USA 104:11130-37
94. Robich RM, Denlinger DL. 2005. Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proc. Natl. Acad. Sci. USA 102:15912-17
95. Rosen L. 1988. Further observations on the mechanisms of vertical transmission by Aedes mosquitoes. Am. J. Trop. Med. Hyg. 39:123-26
96. Rund SS, Lee SJ, Bush BR, Duffield GE. 2012. Strain-And sex-specific differences in daily flight activity and the circadian clock of Anopheles gambiae mosquitoes. J. Insect Physiol. 58:1609-19
97. Saunders DS. 2002. Insect Clocks. Amsterdam: Elsevier
98. Saunders DS. 2010. Controversial aspects of photoperiodism in insects and mites. J. Insect Physiol. 56:1491-502
99. Schmidt PS, Paaby AB, Heschel MS. 2005. Genetic variance for diapause expression and associated life histories in Drosophila melanogaster. Evolution 59:2616-25
100. Shroyer DA, Craig GB. 1983. Egg diapause in Aedes triseriatus (Diptera, Culicidae): Geographic variation in photoperiodic response and factors influencing diapause termination. J. Med. Entomol. 20:601-7
101. Sim C, Denlinger DL. 2008. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl. Acad. Sci. USA 105:6777-81
102. Sim C, Denlinger DL. 2009. A shut-Down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens. Insect Mol. Biol. 18:325-32
103. SimC,DenlingerDL. 2009. Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. Physiol. Genomics 39:202-9
104. Sim C, Denlinger DL. 2011. Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J. Insect Physiol. 57:628-34
105. Sim C, Denlinger DL. 2013. Juvenile hormone III suppresses forkhead of transcription factor in the fat body and reduces fat accumulation in the diapausing mosquito, Culex pipiens. Insect Mol. Biol. 22:1-11
106. Sota T. 1994. Larval diapause, size and autogeny in the mosquito Aedes togoi (Diptera, Culicidae) from tropical to subarctic zone. Can. J. Zool. 72:1462-68
107. Sota T, Mogi M. 1992. Survival time and resistance to desiccation of diapause and non-Diapause eggs of temperate Aedes (Stegomyia) mosquitoes. Entomol. Exp. Appl. 63:155-61
108. Spielman A. 1974. Effect of synthetic juvenile hormone on ovarian diapause of Culex pipiens mosquitoes. J. Med. Entomol. 11:223-25
109. Spielman A, Wong J. 1973. Environmental control of ovarian diapause in Culex pipiens. Ann. Entomol. Soc. Am. 66:905-7
110. Summa K, Urbanski JM, Zhao X, Poelchau MF, Armbruster P. 2012. Cloning and sequence analysis of the circadian clock genes period and timeless in Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 49:777-82
111. Tauber MJ, Tauber CA, Masaki S. 1986. Seasonal Adaptations of Insects. New York, NY: Oxford of insect diapause. Univ. Press
112. Urbanski J, Mogi M, O'Donnell D, DeCotiis M, Toma T, Armbruster P. 2012. Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am. Nat. 179:490-500
113. Urbanski JM, Benoit JB, Michaud MR, Denlinger DL, Armbruster P. 2010. The molecular basis of increased desiccation resistance during diapause in the Asian tiger mosquito, Aedes albopictus. Proc. R. Soc. B 277:2683-92
114. VinogradovaEB. 2000. Culex pipiens pipiens Mosquitoes:Taxonomy, Distribution, Ecology, Physiology, Genetics, Applied Importance and Control. Sofia, Bulgaria: PenSoft
115. Vinogradova EB. 2007. Diapause in aquatic insects, with emphasis on mosquitoes. In Diapause in Aquatic Invertebrates, ed. VR Alekseev, B De Stasio, JJ Gilbert, pp. 83-113. London: Springer
116. Williams KD, Schmidt PS, Sokolowski MB. 2010. Photoperiodism in insects: Molecular basis and consequences of diapause. In Photoperiodism: The Biological Calendar, ed. RJ Nelson, DL Denlinger, DE Somers, pp. 287-317. New York, NY: Oxford Univ. Press
117. Wilton DP, Smith GC. 1985. Ovarian diapause in three geographic strains of Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 22:524-28
118. Yaro AS, Traore A, Huestis DL, Adamou A, Timine S, et al. 2012. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 58:1050-59
119. Zhang Q, Denlinger DL. 2011. Molecular structure of the prothoracicotropic hormone gene in the northern house mosquito, Culex pipiens, and its expression analysis in association with diapause and blood feeding. Insect Mol. Biol. 20:201-13
120. Zhang QR, Denlinger DL. 2011. Elevated couch potato transcripts associated with adult diapause in the mosquito Culex pipiens. J. Insect Physiol. 57:620-27
121. Zhou GL, Miesfeld RL. 2009. Energy metabolism during diapause in Culex pipiens mosquitoes. J. Insect Physiol. 55:40-46